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Original Article

Invitro antioxidant and antibacterial

activities of Xanthium strumarium L.
extracts on methicillinsusceptible and
methicillinresistant Staphylococcus aureus
Javad Sharifi Rad1,2, Seyedeh Mahsan Hoseini Alfatemi3, Majid Sharifi Rad4, Marcello Iriti5
Zabol Medicinal Plants Research Center, Zabol University of Medical Sciences, Zabol, Iran, 2Department of Pharmacognosy, Faculty
of Pharmacy, Zabol University of Medical Sciences, Zabol, Iran, 3Department of Bacteriology and Virology, Shiraz Medical School,
Shiraz University of Medical Sciences, Shiraz, Iran, 4Department of Range and Watershed Management, Faculty of Natural Resources,
University of Zabol, Zabol, Iran, 5Department of Agricultural and Environmental Sciences, Milan State University, via G. Celoria 2,
20133, Milan, Italy
1

ABSTRACT
Background and Aims: The excessive and repeated use
of antibiotics in medicine has led to the development of
antibioticresistant microbial strains, including Staphylococcus
aureus whose emergence of antibioticresistant strains
has reduced the number of antibiotics available to treat
clinical infections caused by this bacterium. In this study,
antioxidant and antimicrobial activities of methanolic
extract of Xanthium strumarium L. leaves were evaluated
on methicillin susceptibleand methicillinresistant
Staphylococcusaureus(MRSA) spp.
Materials and Methods: Antiradical and antioxidant activities
X. strumarium L. leaf extract were evaluated based on its ability
to scavenge the synthetic 1,1diphenyl2picrylhydrazyl(DPPH)
free radical and by the paired diene method, respectively,
whereas the antimicrobial activity was assayed by the disc
diffusion method.
Statistical Analysis: Data were subjected to analysis of variance
following an entirely random design to determine the least
significant difference at P<0.05 using SPSS v. 11.5.
Results and Conclusions: The IC 50 values of the extract
were 0.02mg/mL and 0.09mg/mL for the antioxidant and
DPPHscavenging capacity, respectively. X. strumarium extract
affected both methicillinsensitive Staphylococcusaureus
and MRSA, though antibacterial activity was more effective
on methicillinsusceptible S. aureus spp. The antibacterial
and antioxidant activities exhibited by the methanol extract
may justify the traditional use of this plant as a folk remedy
worldwide.

INTRODUCTION

any medicinal plants are considered as important

natural remedies for the treatment of various
diseases. The excessive and repeated use of some
synthetic drugs in modern medicine has led to the
development of antibioticresistant microbial strains,
including Staphylococcus aureus. [1] The emergence of
antibioticresistant strains of this bacterium reduces
the number of antibiotics available to treat clinical
infections caused by this pathogen.[2] S. aureus is a highly
variable pathogen with considerable impact on human
health. It is responsible for a wide range of hospital
and communityacquired infections globally, from skin
infections and food poisoning to lifethreatening conditions
such as toxicshock syndrome, endocarditis, pneumonia,
bacteremia, and osteomyelitis.[3,4]
Xanthium strumarium L. is an annual plant belonging to
the family Asteraceae. In Iran, X. strumarium is available
between August and September. In many countries,
different plant parts, especially fruit and root, are
used as remedies. Various parts of this plant species
were found to possess useful medicinal properties
such as antitrypanosomal,[5] diuretic,[6] hypoglycemic,[7]
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KEY WORDS: 1,1diphenyl2picrylhydrazyl, antioxidant activity,

methicillinresistant Staphylococcusaureus, methicillinsensitive
Staphylococcusaureus, Staphylococcusaureus, Xanthium
strumarium L

Ancient Science of Life / Oct-Dec 2013 / Vol 33 / Issue 2

www.ancientscienceoflife.org
DOI:
10.4103/0257-7941.139050

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Rad, etal.: Antioxidant and antibacterial activities of Xanthium strumarium L. extracts

a n t h e l m i n t i c , [8] a n t i f u n g a l , [9] a n t i l e i s h m a n i a l , [9]

antiulcerogenic,[10] and antiinflammatory[11,12] activities,
it is also known to inhibit proliferation of human cancer
cells in vitro[13] and to exert a neuroprotective activity on
the central nervous system.[14]

U2001 spectrophotometer (Tokyo, Japan). Antioxidant

activity was measured as follows:

The chemical constituents of X. strumarium include phenolic

compounds such as ferulic acids, chlorogenic acids and
thiazolidinediones; [15] caffeic acid, 1,3,5triOcaffeoyl
quinic acid and 1,5diOcaffeoyl quinic acid;[16] isoprenoids
as sitosterol and strumasterol; [17] monoterpene and
sesquiterpene hydrocarbons;[17] xanthanolide sesquiterpene
lactones [18] and triterpenoid saponins. [19] In addition,
Srinivas etal.[20] reported, high levels of alkaloids, phenolic
acids, and diterpenes and significant concentrations of
saponins, glycosides, fixed oils, and phytosterols in X.
strumarium.[20] The main aim of the present study was
to carry out invitro tests on X. strumarium from Iran by
to assess the antioxidant and antimicrobial activities of
methanolic leaf extracts.

IC50 value(mg/mL) is the efficient concentration at which

the antioxidant capacity was inhibited by 50%, and was
gained by interpolation from linear regression analysis
Analyses were repeated 3 times (technical replicates).
tocopherol, butylated hydroxyanisole(BHA) and ascorbic
acid(SigmaAldrich, USA) were used as standard controls.

MATERIALS AND METHODS

Plant material and extract
Leaves of X. strumarium were collected between August
and September 2012 from the area of Hamun Lake of Zabol
(31 1 43 N, 61 30 4 E), Sistan and Baluchestan Province,
Iran. The plant was taxonomically identified by a botanist
at the herbarium of Department of Botany, Shahid Beheshti
University, Iran. 20 g of dried leaves were and extracted in
200mL 85% methanol using a shaker water bath for 24h
at 25C. After filtration with Whatman No.1 filter paper,
filtrate was concentrated by a rotary evaporator at 50C for
30min., to remove solvent from the extract. Solid extract
was dissolved in 20 mL of distilled water. This working
solution was used for all tests in this study.

Antioxidant activity
Antioxidant activity was determined by the paired diene
method.[21] The antioxidant activity measured represents
the capacity of the plant extract to inhibit the peroxidation
of linoleic acid, in which the double bond is changed to
a paired diene. Each extract sample (0.01-30 mg/mL) in
methanol(100 L) was blended with 3mL of 10 mM linoleic
acid(Sigma Chemical Co., St. Louis, MO, USA) to form an
emulsion in 0.2 M sodium phosphate buffer (pH 6.6) in
test tubes, and then placed in the dark at 37C to stimulate
oxidation. After incubation for 17h, 7mL of 70% methanol
in deionized water was added, and the absorbance of the
mixture was measured at 234nm against a blank in a Hitachi
108

Antioxidant activity (%) = [(A234 of control A234 of

sample)/A234 of control] 100.

Scavenging ability on 1,1diphenyl2picrylhydrazyl

(DPPH) radicals
The scavenging ability on the synthetic (DPPH, Sigma)
free radical, determined according to Shimada etal.,[22] is
the capability of the extract to respond rapidly with DPPH
radicals and to scavenge most DPPH radical molecules.
The test was repeated 3 times. tocopherol, BHA and
ascorbic acid(SigmaAldrich, USA) were used as standards.
Avolume of 5mL of the methanolic extract(0.5-40mg/mL)
was mixed with 1 mL of methanolic solution containing
DPPH radicals, resulting in a final concentration of 0.2 mM
DPPH. The mixture was shaken vigorously, left to stand for
40min., in the dark, and the absorbance was read at 517nm
against a blank. The scavenging ability was determined as
follows:
Scavenging ability (%) = [(A 517 of control A 517 of
sample)/A517 of control] 100.
IC50 value(mg/mL) is the efficient concentration at which
the antioxidant activity was inhibited by 50% and DPPH
radicals were scavenged by 50%, and was gained by
interpolation from linear regression analysis.

Bacterial isolates
The S. aureus strains used in this study were clinical isolates
from patients with S. aureus infections, obtained from the
Microbiological Laboratory of the Central Hospital in Zabol,
Iran. Isolated were identified by biochemical (catalase,
coagulase and DNase) and molecular tests. Isolated
methicillinresistant Staphylococcusaureus(MRSA) were
identified by screening tests on MuellerHinton agar(MHA,
Torlak, Berlin, Germany) complemented with 5% NaCl and
1 mg/mL oxacillinimpregnated disc.[23] The two strains
used in this study were ATTC 25923 (MRSA) and PTCC
1341(MSSA).

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Rad, etal.: Antioxidant and antibacterial activities of Xanthium strumarium L. extracts

Antimicrobial tests were carried out by the disc diffusion

method using 100 L of bacteria suspension (containing
2.0108 CFU/mL of bacteria) dispersed on MHA in sterilized
Petri dishes (60 mm in diameter). To the discs (6 mm in
diameter, HI Media Laboratories Pvt. Ltd., Mumbai, India)
placed on the inoculated agar, 50, 100, 200, and 300 L
of leaf extracts were added. The inoculated plates were
maintained at 4C for 2h and later incubated at 37C for
24h. Antimicrobial activity was determined by measuring
the zone of inhibition(mm) against the test bacterial(MRSA
and MSSA) strains.

Statistical analysis
The extract was prepared in triplicate for antioxidant
and antibacterial tests. Data were subjected to analysis of
variance following an entirely random design to determine
the least significant difference at P<0.05, using statistical
software package (SPSS, version 11.5, IBM Corporation,
NY, USA). All results are expressed as mean standard
deviation.

RESULTS
The results on antioxidant and antiradical activities of the
tested extract are summarized in Table1. The levels of both
antioxidant and DPPH radical scavenging capacities are
inversely correlated with their IC50 values. The IC50 values
of antioxidant activity were 0.04, 0.06, 3.12, and 0.02mg/mL
for tocopherol, BHA, ascorbic acid and X. strumarium leaf
extract, respectively. For the radical scavenging capacity, IC50
values were 1.01, 0.27, 4.01, and 0.09mg/mL for tocopherol,
BHA, ascorbic acid and X. strumarium extract, respectively. In
both assays, activity of X. strumarium methanol extract was
significantly higher than that of the three tested reference
compounds(P<0.05)[Table1]. The results of antibacterial
activity of the leaf extract are shown in Figures1 and 2. Our
result showed that inhibition zones for MSSA(PTCC 1341)
Table1: IC50 values(mg/mL) of the X. strumarium leaf extract
in two tests: Paired diene method and DPPH radical scavenging
assay
Samples
Antioxidant activity DPPH scavenging capacity
X. strumarium extract
0.020.00d
0.090.01d
c
tocopherol
0.040.04
1.010.01b
b
BHA
0.060.00
0.270.00c
a
Ascorbic acid
3.120.00
4.010.00a
Results are meanSD of three replicates; means with different letters within a
column are significantly different (P<0.05; LSD). BHA: Butylated hydroxyanisole,
X. strumarium: Xanthium strumarium, DPPH: 1,1diphenyl2picrylhydrazyl,
SD: Standard deviation, LSD: Least significant difference test at P<0.05

bacteria were 12.110.12(f), 16.080.14(d), 23.060.04(b),

and 26.000.00(a) mm at concentrations of 50, 10, 200, and
300 L of plant extract, respectively(P<0.05)[Figure1]. The
inhibition zones for MSSA isolates were 11.01 0.03 (g),
14.030.00(e), 18.060.14(c), and 26.0.10.02(a) mm,
at concentrations of 50, 10, 200, and 300 L of plant
extract, respectively(P<0.05)[Figure1]. Inhibition zones
relative to MRSA(ATTC 25923) strain were 8.110.00(e),
12.110.11(c), 15.010.00(b), and 18.40.07(a) mm at
concentrations of 50, 10, 200, and 300 L of plant extracts,
respectively(P<0.05)[Figure2]. Inhibition areas obtained for
MRSA isolates were 6.40.2(f), 8.120.01(d), 12.20.5(c),
and 17.80.9(b) mm, at concentrations of 50, 10, 200, and
300 L of plant extracts, respectively(P<0.05)[Figure2].
Our results showed a doseresponse correlation between the
plant extract concentration and the inhibition of bacterial
growth.

DISCUSSION
According to the European Antimicrobial Surveillance
System, MRSA represents currently a huge burden for many
healthcare institutions and it is by far the most significant
antibioticresistant acquired pathogen worldwide.
In previous studies, ethanol extracts from leafs of
Eremophila alternifolia (Myoporaceae), Eremophila
duttonii R.Br. (Myoporaceae), Amyema quandong (Lindl.)
Tiegh.(Loranthaceae) and from the stem base of Lepidosperma
viscidum R.Br. (Cyperaceae), traditional Australian
medicinal plants, showed antibacterial activity against
MRSA.[24] Essential oils of Thymus vulgaris L.(Lamiaceae),
Eucalyptus globulus Labill. (Myrtaceae) [25] and Sinapis

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Figure1: Antibacterial activity of Xanthium strumarium leaf extract against methicillinsensitive Staphylococcusaureus(MSSA)
standard (PTCC 1341) and the clinical isolate MSSA(n=15) measured
as diameter of the zone of inhibition(mm). Different letters indicate
significant differences according to the least significant difference test
at P<0.05. All results are expressed as meanstandard deviation

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Figure2: Antibacterial activity of Xanthium strumarium leaf extracts against methicillinresistant Staphylococcusaureus(MRSA)
standard (ATTC 25923) and the clinical isolate MRSA(n=20) measured as diameter of the zone of inhibition(mm). Different letters indicate significant differences according to the least significant difference
test at P<0.05. All results are expressed as meanstandard deviation

arvensis L. (Brassicaceae)[26] were also effective against

clinical isolates of MRSA in disc diffusion assay. More
recently, antimicrobial activity of essential oil of Daucus
crinitus was reported with the same method, even if
resistance or sensitivity to methicillin of S. aureus strains
used were not specified by authors.[27] As regards X.
strumarium, a methanol leaf extract exhibited a significant
inhibitory activity on the growth of S. aureus,[28] and similar
results were reported on chloroform and ethanol fractions
from X. strumarium leaves.[29] Again, in both studies, the
sensitivity to methicillin of the isolates was not specified.[28,29]
Interestingly, chlorhexidine gluconate(1% and 4%) exerted
a high biocide activity on both MSSA and MRSA.[30]
Our results showed that the maximum concentration of
the extract (300 L) was inhibitory both against MSSA
and MRSA strains, with the highest inhibition zones of
25 mm and 20 mm, respectively. The inhibitory activity
of the plant extract against MSSA was higher than against
MRSA, i.e.in other words, X. strumarium exerted a higher
antimicrobial effect on MSSA than on MRSA. Antibacterial
activity of the methanol extract of X. strumarium leaves
was previously reported by Srinivas etal.[20] and ascribed
to the main components, alkaloids, phenolic acids, and
saponins, phytochemicals with wellknown antimicrobial
properties.[30]
1,1diphenyl2picrylhydrazyl assay is a sensitive method
widely used to assess the free radical scavenging activity
of plant extracts or isolated phytochemicals. DPPH is a
stable free radical which accepts an electron or hydrogen
radical to turn into a stable diamagnetic molecule.[31,32]
This test possesses many advantages compared with other
methods, such as good stability, sensitivity, feasibility, and
110

handiness.[33] Antioxidant activity was expressed as the

IC50(mg/mL), which is the effective concentration at which
the antioxidant activity was inhibited by 50%, gained by
interpolation from linear regression analysis. Very recently,
Kamboj et al.[34] have reported that, among all different
organs of X. strumarium, leaf ethanol extract, with high
levels of phenolics and the highest amount of flavonoids,
showed the highest antioxidant activity. Finally, the relevant
antioxidant and antiradical capacities of X. strumarium
suggest a potential use for the prevention and treatment of
diseases correlated with oxidative stress.

CONCLUSION
The antibacterial activity may be possibly attributed
to the presence of phenolic acids, flavonoids, tannins
and triterpinoids in the methanol extract, as reported
in literature. The antibacterial and antioxidant activities
exhibited by the methanol extract may justify the traditional
use of this plant as folk remedy worldwide. X. strumarium
has emerged as a relevant medicinal plant by virtue of its
documented biological properties and possible applications.

ACKNOWLEDGMENT
The authors are very grateful to Department of Range and
Watershed Management, Faculty of Natural Resources, University
of Zabol for financial support.

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Address for correspondence:

Seyedeh Mahsan Hoseini Alfatemi,

Department of Bacteriology and Virology,
Shiraz Medical School, Shiraz University of
Medical Sciences, Shiraz, Iran.
Email:m.hoseinialfatemi@gmail.com

How to cite this article: Rad JS, Alfatemi SH, Rad MS, Iriti M. In-vitro
antioxidant and antibacterial activities of Xanthium strumarium L. extracts
on methicillin-susceptible and methicillin-resistant Staphylococcus aureus.
Ancient Sci Life 2013;33:107-11.
Source of Support: The authors are very grateful to

Department of Range and Watershed Management, Faculty

of Natural Resources, University of Zabol for financial support.
Conflict of Interest: None declared.

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